enemy release hypothesis

Ecologists have identified many potential reasons for the success of invasive species, including higher growth rates or seed production than native species, more aggressive dispersal, tolerance of environmental heterogeneity, more efficient use of resources, and phenological advantages such as an earlier or longer flowering season.{{Cite journal|last1=Estoup|first1=Arnaud|last2=Guillemaud|first2=Thomas|date=2010-08-13|title=Reconstructing routes of invasion using genetic data: why, how and so what?|journal=Molecular Ecology|language=en|volume=19|issue=19|pages=4113–4130|doi=10.1111/j.1365-294X.2010.04773.x|pmid=20723048|bibcode=2010MolEc..19.4113E |s2cid=8242098|doi-access=free}}{{Cite book|title=Biological invasions|last1=Pysek|first1=Petr|last2=Richardson|first2=David M.|date=2007|publisher=Springer|others=Nentwig, Wolfgang, 1953-|isbn=978-3-540-36920-2|editor-last=Nentwig|editor-first=Wolfgang|volume=193|location=Berlin|pages=97–125|chapter=Traits associated with invasiveness in alient plants: Where do we stand?|oclc=184984594}}{{Cite journal|last1=van Kleunen|first1=Mark|last2=Weber|first2=Ewald|last3=Fischer|first3=Markus|date=2010|title=A meta-analysis of trait differences between invasive and non-invasive plant species|journal=Ecology Letters|language=en|volume=13|issue=2|pages=235–245|doi=10.1111/j.1461-0248.2009.01418.x|pmid=20002494|url=https://kops.uni-konstanz.de/bitstreams/bd1d9b68-039f-4083-a531-34d0f7780090/download}} Invasive species may have greater phenotypic plasticity in important traits than their native competitors, allowing them to tolerate more environmental variation,{{Cite journal|last1=Davidson|first1=Amy Michelle|last2=Jennions|first2=Michael|last3=Nicotra|first3=Adrienne B.|date=2011|title=Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis: Invasive species have higher phenotypic plasticity|journal=Ecology Letters|language=en|volume=14|issue=4|pages=419–431|doi=10.1111/j.1461-0248.2011.01596.x|pmid=21314880|doi-access=}} or exhibit the ability to evolve rapidly to adapt to their new conditions.{{Cite journal|last1=Whitney|first1=Kenneth D.|last2=Gabler|first2=Christopher A.|date=2008-04-15|title=Rapid evolution in introduced species, 'invasive traits' and recipient communities: challenges for predicting invasive potential: Evolution and invasion predictions|journal=Diversity and Distributions|language=en|volume=14|issue=4|pages=569–580|doi=10.1111/j.1472-4642.2008.00473.x|doi-access=free}} In addition, some habitats, due to disturbances or other factors, may be more vulnerable to invasion than others.{{Cite book|title=Ecology of invasive plants: state of the art|last1=Rejmanek|first1=M.|last2=Richardson|first2=David M.|publisher=Blackwell|year=2005|editor-last=Van der Marl|editor-first=E.|location=Oxford, England|pages=332–355|chapter=Plant invasion and the invasibility of plant communities|editor-last2=Franklin|editor-first2=J.}} Most exotic species do not become invasive,{{Cite journal|last1=Williamson|first1=Mark|last2=Fitter|first2=Alastair|date=1996|title=The Varying Success of Invaders|journal=Ecology|language=en|volume=77|issue=6|pages=1661–1666|doi=10.2307/2265769|jstor=2265769|bibcode=1996Ecol...77.1661W }} and some authors suggest that those that do represent repeated and larger introductions that generate propagule pressure.{{Cite journal|last=Simberloff|first=Daniel|date=2009|title=The Role of Propagule Pressure in Biological Invasions|journal=Annual Review of Ecology, Evolution, and Systematics|language=en|volume=40|issue=1|pages=81–102|doi=10.1146/annurev.ecolsys.110308.120304|s2cid=85842323 |issn=1543-592X}} Among the many explanations for invasive success, however, the enemy release hypothesis has had the most support.{{Cite journal|last1=Flory|first1=S. Luke|last2=Clay|first2=Keith|date=2013|editor-last=Thrall|editor-first=Peter|title=Pathogen accumulation and long‐term dynamics of plant invasions|journal=Journal of Ecology|language=en|volume=101|issue=3|pages=607–613|doi=10.1111/1365-2745.12078|s2cid=86845671 |issn=0022-0477|doi-access=}}

The enemy release hypothesis (ERH) is most often applied to invasive plants, but there is evidence for its usefulness in other systems, including fish,{{Cite journal|last1=Sarabeev|first1=Volodimir|last2=Balbuena|first2=Juan Antonio|last3=Morand|first3=Serge|date=2017|title=Testing the enemy release hypothesis: abundance and distribution patterns of helminth communities in grey mullets (Teleostei: Mugilidae) reveal the success of invasive species|journal=International Journal for Parasitology|language=en|volume=47|issue=10–11|pages=687–696|doi=10.1016/j.ijpara.2017.05.006|pmid=28694188}} amphibians,{{Cite journal|last1=Marr|first1=Shenandoah R.|last2=Mautz|first2=William J.|last3=Hara|first3=Arnold H.|date=2008|title=Parasite loss and introduced species: a comparison of the parasites of the Puerto Rican tree frog, (Eleutherodactylus coqui), in its native and introduced ranges|journal=Biological Invasions|language=en|volume=10|issue=8|pages=1289–1298|doi=10.1007/s10530-007-9203-0|bibcode=2008BiInv..10.1289M |s2cid=43072717|issn=1387-3547}} insects,{{Cite journal|last1=Aliabadi|first1=Brianna W.|last2=Juliano|first2=Steven A.|title=Escape from gregarine parasites affects the competitive interactions of an invasive mosquito|date=2002|journal=Biological Invasions|volume=4|issue=3|pages=283–297|doi=10.1023/A:1020933705556|pmc=2748405|pmid=19777120}} and crustaceans.{{Cite journal|last1=Torchin|first1=Mark E.|last2=Lafferty|first2=Kevin D.|last3=Kuris|first3=Armand M.|date=2001|title=Release from parasites as natural enemies increased performance of a globally introduced marine crab|journal=Biological Invasions|volume=3|issue=4|pages=333–345|doi=10.1023/A:1015855019360|s2cid=9445764}} The ERH assumes that: (1) herbivores, pathogens and parasites suppress plant population growth, (2) these enemies plague native plants more than immigrating non-native species, and (3) non-native plants are able to leverage this advantage into more rapid population growth.{{Cite journal|last1=Keane|first1=R|last2=Crawley|first2=MJ|date=2002-04-01|title=Exotic plant invasions and the enemy release hypothesis|journal=Trends in Ecology & Evolution|volume=17|issue=4|pages=164–170|doi=10.1016/S0169-5347(02)02499-0}}

An early study of the flowering plant Silene latifolia found that about 60% of its invasive populations in North America were free from herbivory, while 84% of those in its native Europe exhibited damage from at least one herbivore.{{Cite journal|last=Wolfe|first=Lorne M.|date=2002|title=Why Alien Invaders Succeed: Support for the Escape‐from‐Enemy Hypothesis|journal=The American Naturalist|language=en|volume=160|issue=6|pages=705–711|doi=10.1086/343872|pmid=18707459|s2cid=205984290|issn=0003-0147}} A study of almost 500 exotic plant species in the United States found that they were infected by 84% fewer fungi and 24% fewer virus species than in their native ranges.{{Cite journal|last1=Mitchell|first1=Charles E.|last2=Power|first2=Alison G.|date=2003|title=Release of invasive plants from fungal and viral pathogens|journal=Nature|language=en|volume=421|issue=6923|pages=625–627|doi=10.1038/nature01317|pmid=12571594|issn=0028-0836|bibcode=2003Natur.421..625M|s2cid=4320245}} And a meta-analysis covering 15 exotic plant studies found the number of insect herbivores on average to be greater in their native than in their introduced range, with overall damage greater on native plants than on the introduced species.{{Cite journal|last1=Liu|first1=Hong|last2=Stiling|first2=Peter|date=2006|title=Testing the enemy release hypothesis: a review and meta-analysis|journal=Biological Invasions|language=en|volume=8|issue=7|pages=1535–1545|doi=10.1007/s10530-005-5845-y|bibcode=2006BiInv...8.1535L |s2cid=35919248|issn=1387-3547|citeseerx=10.1.1.453.9744}}

Support for the theory, however, is not universal.{{Cite journal|last1=Jeschke|first1=Jonathan|last2=Gómez Aparicio|first2=Lorena|last3=Haider|first3=Sylvia|last4=Heger|first4=Tina|last5=Lortie|first5=Christopher|last6=Pyšek|first6=Petr|last7=Strayer|first7=David|date=2012-08-22|title=Support for major hypotheses in invasion biology is uneven and declining|journal=NeoBiota|volume=14|pages=1–20|doi=10.3897/neobiota.14.3435|issn=1314-2488|doi-access=free|hdl=10261/56814|hdl-access=free}} In some cases, native pathogens, parasites and herbivores present significant biotic resistance to potential invasive species,{{Cite journal|last1=Parker|first1=Ingrid M.|last2=Gilbert|first2=Gregory S.|date=2007|title=When there is no escape: The effects of natural enemies on native, invasive and non-invasive plants|journal=Ecology|language=en|volume=88|issue=5|pages=1210–1224|doi=10.1890/06-1377|pmid=17536407|bibcode=2007Ecol...88.1210P |s2cid=41013635 |issn=0012-9658}}{{Cite journal|last1=Maron|first1=John L.|last2=Vila|first2=Montserrat|author-link2=Montserrat Vilà |s2cid=17449132|date=2001|title=When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses|journal=Oikos|language=en|volume=95|issue=3|pages=361–373|doi=10.1034/j.1600-0706.2001.950301.x|bibcode=2001Oikos..95..361M |issn=0030-1299}} as do non-native enemies that may have arrived prior to the exotic plant.{{Cite journal|last1=Powell|first1=Kristin I.|last2=Chase|first2=Jonathan M.|last3=Knight|first3=Tiffany M.|date=2011|title=A synthesis of plant invasion effects on biodiversity across spatial scales|journal=American Journal of Botany|language=en|volume=98|issue=3|pages=539–548|doi=10.3732/ajb.1000402|pmid=21613145|url=https://openscholarship.wustl.edu/cgi/viewcontent.cgi?article=1018&context=bio_facpubs}} Enemy release may be weaker, too, when an exotic species is more closely related to native species in their introduced ranges, making them more likely to share herbivores or pathogens.{{Cite journal|last1=Hill|first1=Steven Burton|last2=Kotanen|first2=Peter M.|date=2009|title=Evidence that phylogenetically novel non-indigenous plants experience less herbivory|journal=Oecologia|language=en|volume=161|issue=3|pages=581–590|doi=10.1007/s00442-009-1403-0|pmid=19585153|issn=0029-8549|bibcode=2009Oecol.161..581H|hdl=1807/73981|s2cid=12619010|hdl-access=free}} In a meta-analysis of 19 research studies involving 72 pairs of native and invasive plants, invasive exotic species did not incur less damage than their native counterparts and, in fact, exhibited lower relative growth rates.{{Cite journal|last1=Chun|first1=Young Jin|last2=Van Kleunen|first2=Mark|last3=Dawson|first3=Wayne|date=2010-06-10|title=The role of enemy release, tolerance and resistance in plant invasions: linking damage to performance: Invasive plants and enemy release|journal=Ecology Letters|volume=13|issue=8|language=en|pages=937–46|doi=10.1111/j.1461-0248.2010.01498.x|pmid=20545733|url=http://nbn-resolving.de/urn:nbn:de:bsz:352-124238}} In other cases, invasive success was due not to release from herbivory but greater tolerance of it.{{Cite journal|last1=Ashton|first1=Isabel W.|last2=Lerdau|first2=Manuel T.|date=2007-10-04|title=Tolerance to herbivory, and not resistance, may explain differential success of invasive, naturalized, and native North American temperate vines: Resistance and tolerance of invasive vines|journal=Diversity and Distributions|language=en|volume=14|issue=2|pages=169–178|doi=10.1111/j.1472-4642.2007.00425.x|s2cid=83429134 }}

The ERH is closely related to two other important theories for invasive species success: the evolution of increased competitive ability (EICA) and novel weapons hypotheses (NWH). EICA asserts that because exotic plants are released from the burden of defending themselves against herbivores in their native range, they evolve to reallocate those resources to traits, such as growth and seed production, that make them more formidable competitors in their introduced range.{{Cite journal|last1=Blossey|first1=Bernd|last2=Notzold|first2=Rolf|s2cid=15256369|date=1995|title=Evolution of Increased Competitive Ability in Invasive Nonindigenous Plants: A Hypothesis|journal=The Journal of Ecology|volume=83|issue=5|page=887|doi=10.2307/2261425|jstor=2261425|bibcode=1995JEcol..83..887B }} ERH is an ecological mechanism, while EICA rests on evolutionary adaptation.{{Cite journal|last1=Felker-Quinn|first1=Emmi|last2=Schweitzer|first2=Jennifer A.|last3=Bailey|first3=Joseph K.|date=2013|title=Meta-analysis reveals evolution in invasive plant species but little support for Evolution of Increased Competitive Ability (EICA)|journal=Ecology and Evolution|language=en|volume=3|issue=3|pages=739–751|doi=10.1002/ece3.488|pmc=3605860|pmid=23531703}} The experimental support for EICA is mixed.{{Cite journal|last1=Joshi|first1=J.|last2=Vrieling|first2=K.|date=2005-04-28|title=The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores: Evolutionary change in invasive ragwort|journal=Ecology Letters|language=en|volume=8|issue=7|pages=704–714|doi=10.1111/j.1461-0248.2005.00769.x}} For example, Solidago altissima plants artificially released from herbivory became more competitive against other plant species.{{Cite journal|last1=Uesugi|first1=Akane|last2=Kessler|first2=André|date=2013|title=Herbivore exclusion drives the evolution of plant competitiveness via increased allelopathy|journal=New Phytologist|language=en|volume=198|issue=3|pages=916–924|doi=10.1111/nph.12172|pmid=23437810|doi-access=free}} However, a meta-analysis of 30 studies that found evidence of evolutionary shifts in introduced species, showed no indication of a trade-off between herbivore defenses and growth.

The novel weapons hypothesis (NWH) is another perspective on the enemy release hypothesis. Some plants evolve chemical defenses to compete in their original range. In their introduced range, the native species are highly vulnerable to these chemicals because they have no prior experience with them, giving the exotic species a competitive advantage.{{Cite journal|last1=Callaway|first1=Ragan M.|last2=Ridenour|first2=Wendy M.|last3=Laboski|first3=Trevor|last4=Weir|first4=Tiffany|last5=Vivanco|first5=Jorge M.|date=2005|title=Natural selection for resistance to the allelopathic effects of invasive plants|journal=Journal of Ecology|language=en|volume=93|issue=3|pages=576–583|doi=10.1111/j.1365-2745.2005.00994.x|bibcode=2005JEcol..93..576C |issn=0022-0477|doi-access=free}}{{Cite journal|last1=Cappuccino|first1=Naomi|last2=Arnason|first2=J.Thor|date=2006|title=Novel chemistry of invasive exotic plants|journal=Biology Letters|language=en|volume=2|issue=2|pages=189–193|doi=10.1098/rsbl.2005.0433|issn=1744-9561|pmc=1618907|pmid=17148359}}{{Cite journal|last1=Inderjit|last2=Callaway|first2=Ragan M.|last3=Vivanco|first3=Jorge M.|date=2006|title=Can plant biochemistry contribute to understanding of invasion ecology?|journal=Trends in Plant Science|language=en|volume=11|issue=12|pages=574–580|doi=10.1016/j.tplants.2006.10.004|pmid=17092763}}

A final argument for the ERH lies in the success of biological control of some invasive species, in which herbivores or other enemies from their native environment are introduced to suppress population growth in their adopted range.{{Cite journal|last1=Clewley|first1=Gary D.|last2=Eschen|first2=René|last3=Shaw|first3=Richard H.|last4=Wright|first4=Denis J.|date=2012|editor-last=Sheppard|editor-first=Andy|title=The effectiveness of classical biological control of invasive plants|journal=Journal of Applied Ecology|language=en|volume=49|issue=6|pages=1287–1295|doi=10.1111/j.1365-2664.2012.02209.x|bibcode=2012JApEc..49.1287C }} For example, when conservationists sought to control the invasive St.-John's-wort (Hypericum perforatum) in North America, they imported a leaf herbivore (Chrysolina quadrigemina) from its native range in Europe.{{Cite book|title=Assessment and Management of Plant Invasions|last=DeLoach|first=C.J.|date=1997|publisher=Springer New York|isbn=978-1-4612-1926-2|editor-last=Luken|editor-first=James O.|location=New York |pages=172–194|chapter=Biological control of weeds in the United States and Canada|oclc=840278263|editor-last2=Thieret|editor-first2=John W.}}

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Category:Population ecology

Category:Invasive species